A review and illustrated description of Musca crassirostris

Medical and Veterinary Entomology (2019) 33, 16–30 doi: 10.1111/mve.12339 REVIEW ARTICLE A review and illustrated description of Musca crassirostris, one of the most neglected haematophagous livestock flies M. D E S Q U E S N E S 1,2,3, S. O N J U 4, P. C H A L E R M W O N G 3, S. J I T T A P A L A P O N G 5 and R. M A S M E A T A T H I P 4 1Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), Unité Mixte de Recherche (UMR) InterTryp, Bangkok, Thailand, 2InterTryp, Institut de Recherche pour le Développement (IRD), CIRAD, University of Montpellier, Montpellier, France, 3Department of Parasitology, Faculty of Veterinary Medicine, Kasetsart University, Bangkok, Thailand, 4Department of Entomology, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Nakhon Pathom, Thailand and 5Faculty of Veterinary Technology, Kasetsart University, Bangkok, Thailand Abstract. Tabanids, stomoxyine flies, hippoboscids and tsetse flies are the most well-known brachyceran biting flies of livestock. Only a few other higher Diptera have developed the unique mouthparts required for blood feeding. These neglected blood feeders can also have direct effects on hosts through blood loss, and are likely to contribute to the transmission of pathogens. Musca crassirostris (Diptera: Muscidae) is one of the most abundant of the muscid flies with this haematophagous lifestyle; it is widespread in the Palaearctic, Afrotropical and Oriental regions. The present study reviews and summarizes the biology and morphology of this species, and its potential for impact on animals and humans. The study also provides a fully illustrated description of the fly to facilitate its identification, and reviews information on abundance, with a focus on recent trapping surveys in Thailand. When sampled using traps designed for other biting flies, M. crassirostris appears to be four and 45 times more abundant than stomoxyines and tabanids, respectively. High numbers of M. crassirostris in the vicinity of livestock have also been associated with outbreaks of disease, such as that of a fatal plague in bovine farms in Egypt. This calls for a reconsideration of its potential impacts on livestock economics and health, and thus the development of suitable control methods. Key words. Bloodsucking fly, cattle fly, illustration, identification, impact. Introduction Diptera of the genus Musca have evolved the mouthparts required for blood feeding. These neglected blood feeders can Among the many flies annoying livestock, the most well known also have direct effects on hosts through blood loss and through of the haematophagous brachyceran biting flies globally are the mechanical transmission of pathogens (Skidmore, 1985). tabanids, hippoboscids and stomoxyines, which are notably responsible for the mechanical transmission of trypanosomes The family Muscidae is divided into seven subfamilies and such as Trypanosoma vivax and Trypanosoma evansi (Surra) contains about 4500 species in 180 genera (de Carvalho et al., (Kinetoplastida: Trypanosomatidae) (Baldacchino et al., 2013, 2005; Nihei & de Carvalho, 2007). The subfamily Muscinae 2014); tsetse flies [Glossina (Diptera: Glossinidae)] are also contains two tribes of veterinary importance: the Stomoxyini, well known in Africa because they transmit nagana and sleeping which consists of bloodsucking insects such as species within sickness (Bitome Essono et al., 2015). Only a few other higher the genera Stomoxys, Haematobia and Haematobosca, and the Muscini, which contains non-biting insects such as those of Correspondence: Roungthip Masmeatathip, Department of Entomology, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Kamphaeng Saen Campus, Nakhon Pathom 73140, Thailand. Tel.: + 66 34351886; Fax: + 66 34351886; E-mail: [email protected] 16 © 2018 The Authors. Medical and Veterinary Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.

The blood feeder Musca crassirostris 17 the genera Fannia, Hydrotaea, Morellia and the most impor- (Hopla et al., 1994), together with M. planiceps and M. inferior tant Musca (Skidmore, 1985; Nevill, 1997; Nihei & de Car- (Patton & Senior-White, 1924), and thus it should be considered valho, 2007). The genus Musca Linnaeus is cosmopolitan and as an obligate parasite. includes roughly 60 species, at least one of which, Musca domes- tica, is found worldwide as a result of its close association with Musca crassirostris is present in the Palaearctic, Afrotropical humans. The Musca spp. include both anthropophilic ‘house and Oriental regions (Walker, 1994); it is found in Africa, from flies’ (‘sponging flies’, such as M. domestica, Musca nebulo and South Africa to the Mediterranean coast, through the Middle Musca humilis) and less well-known ‘wild flies’. Several species East and India to Asia, including Taiwan and Southeast Asia, are haematophagous (although in some of them this status has and as far as Indonesia (James, 1947; Skidmore, 1985). It is also been subject to controversy), including Musca ventrosa, Musca called the ‘Indian fly’ (Russel et al., 2013), and, as suggested by albomaculata, Musca spinohumera, Musca bezzii, Musca lin- Patton (1922), it could as well be called the ‘cattle fly’ because it eata, Musca inferior, Musca conducens, Musca planiceps and is very abundant around cattle. Most of the authors reporting this Musca crassirostris (Patton, 1922). These species are typically fly mention that it is very abundant on cattle (Patton & Patton, referred to as ‘bloodsucking flies’ rather than ‘biting flies’; in 1920). other words, they are not ‘skin-piercing’ flies. Musca crassirostris Stein, 1903 was also designated Phi- All Musca spp. can feed on liquids containing organic matter laematomyia insignis Austen (Patton & Cragg, 1913), Musca from various substrates (such as organic wastes, excrements, (Philaematomyia) crassirostris, Stein (Patton, 1922), Phi- carcasses, secretions from wounds and sores, and lacrimation laematomyia crassirostris (Stein) and Musca insignis Austen fluids). They may also regurgitate to dampen substrates, or (James, 1947); all these names are now considered synonymous. to dilute coarse or viscous fluids, in order to take up liquids Following Austen, the subgenus Philaematomia was created through the pseudotracheae, or to partially digest materials (as a genus) because of the stout proboscis of crassirostris before ingesting them (Nevill, 1997). Some flies, such as Musca with its prestomal teeth. However, M. inferior, Musca senior pattoni, feed on blood that oozes from punctures made by true whitei and a few other species, which are more or less similar biting flies and are suspected to contribute to the mechanical in this characteristic, were not included in this genus (Van transmission of blood pathogens, such as trypanosomes (Patton, Emden, 1965). As has been clearly stated, and notably based 1922). A number of haematophagous species, such as Musca on the structure of the proboscis, which is similar to that of autumnalis, Musca bezzii, Musca lusoria and others, follow M. domestica, there is no doubt that crassirostris belongs to the the pattern of true skin-piercing, blood-sucking flies (such as genus Musca (Patton, 1932). Stomoxys spp.), which causes them to withdraw the proboscis in order to suck up any blood or serum that commonly exudes from The systematic position of M. crassirostris is: Order Diptera; the bite (Patton, 1932); such flies may land next to a true biting suborder Brachycera; family Muscidae; subfamily Muscinae; fly and push it laterally to dislodge its proboscis from the skin in tribe Muscini; genus Musca, and species crassirostris (Borror order to suck the blood that oozes immediately after proboscis & White, 1970; Skidmore, 1985). removal (MD, personal observation, 2007–2017). The present paper reviews and summarizes the biology and All Musca spp. have one or more circles of prestomal teeth; morphology of M. crassirostris, and its potential for impacts the first row of these prestomal teeth ranges in size and form, on animals and humans. It also provides a fully illustrated according to the species. A moderate development of these description of the fly in order to facilitate its identification, and teeth can allow the fly to scratch the surface of a blood clot; reviews information on its abundance, with a focus on recent in this way, they can ‘refresh’ wounds left at biting sites by trapping surveys in Thailand. true biting insects. This will drain more blood after the bite, as described for Musca lineata or M. conducens (Patton, 1922) Biology of M. crassirostris (also called Philaematomia lineata), and for M. lusoria and M. autumnalis (Nevill, 1997); such behaviour makes them fac- Both adult males and females of M. crassirostris are ultative haematophagous flies (Russel et al., 2013). The mentum haematophagous; males suck blood as voraciously as females and teeth are more strongly chitinized in true blood feeders such (Patton & Cragg, 1913). Some authors do not consider this as M. planiceps (Patton & Senior-White, 1924). This type of fly to be an obligatory parasite, stating that it can survive on proboscis reaches its highest evolution with a strongly chitinized various animal secretions, and, indeed, adult M. crassirostris mentum and fully developed prestomal teeth in M. inferior have also been observed sucking some organic fluids at the and M. crassirostris. These flies are able to abrade the skin surface of fresh cattle dung (Patton & Cragg, 1913). However, of their hosts in order to feed on blood (Patton, 1923; Patton the species is especially attracted by wounds and blood for & Senior-White, 1924), to rasp scabs or wounds, and possi- feeding (Taylor et al., 2007). To feed on blood, M. crassirostris bly to pierce soft skin by injuring epidermal and dermal tis- flies can either make their own lesions by rasping the skin sues (James, 1969; Greenberg 1971, quoted by Skidmore, 1985). with the labella, or can act as secondary blood feeders, either Some authors therefore consider them to be ‘biting flies’ (Mel- by refreshing a biting site by rasping the clot resulting from lor, 1978; Nevill & Sutherland, 1987). Others do not consider the feeding of a true biting fly (tabanid or stomoxyine), or by them to be ‘true’ biting flies as the proboscis does not pene- lapping liquid blood from around wounds or punctures made trate the skin (Patton & Cragg, 1913; Patton & Senior-White, by true bloodsucking flies. For these reasons, some authors 1924; Muirhead Thomson, 1947; Crosskey, 1993). Finally, consider these flies as true blood feeders and even qualify them M. crassirostris belongs to a group of true obligate blood feeders as ‘biting flies’ (Patton & Senior-White, 1924; Hopla et al., © 2018 The Authors. Medical and Veterinary Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society, Medical and Veterinary Entomology, 33, 16–30

18 M. Desquesnes et al. 1994); however, the proboscis of this species does not penetrate complete larval development can occur in as short a period as the skin (Patton & Senior-White, 1924). 1 week and the species may produce several generations per year in temperate climates; in tropical areas, breeding may be contin- This species, although not a stomoxyine, is very similar to uous. Haematobia species (Diptera: Muscidae) in its general biology (Lane & Crosskey, 1993). Gravid females have been observed A study of temperature limits in adults indicated that the on the fresh dung of cows and buffaloes, and sometimes in horse lowest temperatures at which movement of adult flies was dung (Patton & Cragg, 1913). However, in a study carried out in noted averaged 10.4 ∘C; heat paralysis began at 44.9 ∘C and Egypt, eggs were found only in bovine dung and not in the dung was complete at 46.3 ∘C (West, 1951). Studies in Egypt have of equines, camels, sheep, goats, poultry, pigs, rabbits or humans shown that flies are scarce when the temperature is below (Hafez & Gamal-Eddin, 1966). 21 ∘C or above 35 ∘C, but are very abundant at temperatures between 21 ∘C and 30 ∘C (Hafez & Gamal-Eddin, 1966). Like The female is oviparous; before laying eggs, it looks for other haematophagous flies, adults of M. crassirostris have been a crack or crevice in fresh dung into which to insert its shown to be significantly attracted by carbon dioxide (Bernier ovipositor. Within 6–10 min, a female can lay 40–60 large et al., 2008). eggs (2.0–2.2 mm in length, 0.4 mm in breadth) into freshly dropped cattle or horse dung, or some rotting organic material Musca crassirostris may be parasitized by nematodes such as (Patton & Cragg, 1913; West, 1951). Greenberg, quoted by Heterotylenchus crassirostris (Tylenchida: Allantonematidae), Skidmore (1985), refers to the species as a symbovine that which affects the ovaries of females and could potentially be is hemi-synanthropic in some areas. In 1951, Zimin [quoted used for biological control (Yatham & Rao, 1981). However, by Skidmore (1985)] reported up to seven females laying because of the specific affinity of this fly for fresh dung, simultaneously on one cowpat, covering it with masses of especially cattle dung, a simple management technique for fly large eggs. This gregariousness was also observed and carefully control in stables involves the rapid and regular removal of dung. described by Patton & Cragg (1913), who reported up to This will limit the habitat suitable for egg laying and larval 36 females laying 560 eggs in one spot; such gregarious development, but is not practical in the context of free-ranging behaviour is unique among muscids. Gregarious behaviour was livestock. also described in males, which have been observed to swarm in their hundreds in India (Van Emden, 1965). Impact of M. crassirostris on animals and humans These large eggs suggest some early development inside the Reducing the direct impacts of this fly on livestock is a priority uterus (Patton, 1922). Indeed, the eggs of this species hatch very of livestock owners in some areas; for example, cattle deaths quickly after being laid, in 8–9 h or less (Patton & Cragg, 1913); at high abundances have been reported in Egypt (Hafez & this time is so short, compared with that for other Musca spp. (on Gamal-Eddin, 1966). However, indirect impacts linked with average 20 h), that some authors even consider M. crassirostris pathogen transmission should not be neglected. as taking a step towards larviparous behaviour (Patton, 1932), or even as demonstrating ‘facultative viviparity’ as the brief period Direct pathogenic effects between oviposition and larval hatching suggests that all eggs in a batch are retained for some time in the uterus of the female Musca crassirostris was considered as one of the most impor- (Meier et al., 1999). Finally, M. crassirostris is the only muscid tant pests of cattle in India (Patton, 1922). Earlier research species to cumulate haemophagocity and facultative viviparity. recorded huge numbers of these flies on cattle, especially on However, its viviparity is not advanced (James, 1969), and is the legs, which required the cattle to spend a lot of time and nothing to compare with that of M. planiceps, which deposits energy fending off these insects, and concluded that their feed- its larvae one at a time in fresh cow dung in the early third stage, ing behaviour and incredible numbers must significantly reduce after retaining them in utero during two moults (Patton, 1932). milk production (Patton, 1922). In Oman, average numbers of five to 200 flies have been observed on cattle at one time, with The larvae are saprophagous and can be reared to maturity on numbers sometimes exceeding 500 (Mellor, 1978). The animal dung alone. First-instar larvae stay together and feed in the dung stress resulting from visual, aural and tactile harassment must for 24 h and then move deeper into the dung or deeper into the be substantial, even without considering the impacts of all other earth under litter to continue development. Larvae (maggots) are insects annoying livestock. Musca crassirostris most often feeds a deep lemon-yellow colour, and are segmented and cylindrical. on the legs and belly; cattle typically lie down on their legs to The three larval stages feed on decomposing organic material protect themselves from attacks (Patton, 1922). This extreme and mature within 3–7 days under suitable conditions. Mature behaviour has also been seen in French Guyana, where cattle larvae move deeper into the damp soil below cattle dung, or try to escape very high tabanid pressure (Desquesnes, 2004). to drier areas around the larval habitat to pupariate (Mellor, Because of their nuisance effects, flies distract and essentially 1978). In laboratory rearing in Egypt at 25 ∘C and 32 ∘C, limit the time available for normal feeding activity. The result- respectively, development took 11 h and 7 h (eggs), 6.5 days and ing reduction in food intake, combined with the stress and the 3.2 days (larvae) and 6.7 days and 4.0 days (pupae) (Hafez & energy spent on dislodging flies, is the most important effect of Gamal-Eddin, 1966). Complete development took 14 days and M. crassirostris on livestock in pasture. This leads to reduced 8 days at 25 ∘C and 32 ∘C, respectively. Puparia measure 5–10 mm in length and are of a mahogany colour (Patton & Cragg, 1913). Adult flies have been observed to emerge between 3 and 26 days later, depending on the tem- perature (Taylor et al., 2007). Thus, under optimal conditions, © 2018 The Authors. Medical and Veterinary Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society, Medical and Veterinary Entomology, 33, 16–30

The blood feeder Musca crassirostris 19 weight gain in beef cattle, reduced milk production in dairy cat- as Escherichia coli (Enterobacteriales: Enterobacteriaceae), tle, and reduced manure production (Patton, 1922). However, Moraxella bovis (Pseudomonadales: Moraxellaceae) (pink- the specific impact of M. crassirostris on livestock has yet to be eye) and Staphylococcus aureus (Bacillales: Staphylococ- measured independently of the impacts of other flies, including caceae) (Walker, 1994). More importantly, like biting flies, biting flies. M. crassirostris is considered as a mechanical vector of some pathogens; many years ago it was shown to transmit surra and Musca crassirostris attacks mainly cattle, causing severe haemorrhagic septicaemia (Du Toit & Nieschlutz, 1933; Gill, irritation and sometimes weakening the animal so much that 1977). High numbers of pathogens can be transmitted by insects death may result (Hafez & Gamal-Eddin, 1966; Harwood & acting as mechanical vectors (Taylor et al., 2007) and those that James, 1979). may be transmitted by M. crassirostris are unlikely to differ from those recently reviewed for stomoxyines and tabanids (Bal- Musca crassirostris can attack horses and donkeys, although dacchino et al., 2013, 2014). Some examples are viruses such as the species is more usually found on bovines (cattle and equine infectious anaemia virus and lumpy skin disease virus, buffaloes), and it may occasionally attack humans and dogs bacteria such as Bacillus anthracis (Bacillales: Bacillaceae) (Patton & Cragg, 1913; Lane & Crosskey, 1993; Chin et al., and Anaplasma marginale (Rickettsiales: Anaplasmataceae) 2010). It has also been found on camels (Dia, 1997), and on and protozoa such as Besnoitia besnoiti (Eucoccidiorida: tigers and deer, as observed in a natural park in India (Veer et al., Sarcocystidae) and Trypanosoma spp. (notably T. evansi and 2002). Animals in poor condition have more flies than others, T. vivax). which may relate to the exhaustion of these animals, which are no longer able to fend off the insects (Mellor, 1978). In addition, a number of nematodes are suspected or proven to be biologically transmitted by M. crassirostris. All scratching When using the prestomal teeth to rasp the skin, at either a Musca (such as M. senior-whitei, Musca fletcheri, M. planiceps, wound or any altered part of the skin, M. crassirostris is respon- M. inferior and M. crassirostris) are potential transmitters of sible for a painful bite that generates stress that contributes to pathogenic organisms, and M. crassirostris has been consid- immunosuppression in animals; subsequently, when feeding, the ered as a probable transmitter of Habronema spp. (Spirurida: fly is responsible for the depletion of blood, which also impacts Habronematidae) in India as these nematodes were found to animal production. develop in it (Patton, 1932). According to Nevill, (1975), the- oretically M. crassirostris, as well as Haematobia spp. and The sizes of the bloodmeals taken by a number of M. conducens, would all be ideal transmitters of Parafilaria haematophagous flies were established by Gooding (1972). bovicola (Spirurida: Filariidae) because they are able to lap up Based on his estimates, and the size of the insect, the bloodmeal infected blood and later infect animals through the wounds they of M. crassirostris amounts to about 10–40 mg per fly [the cause by their own feeding; however, experimental evidence is closest size is Stomoxys calcitrans, which takes a bloodmeal of lacking. 7–25 mg (Gooding, 1972)]. In a situation in which more than 500 M. crassirostris may attack one cow (Mellor, 1978), the Thelazia (Spirurida: Thelaziidae) are eyeworms. Adult worms blood depletion of cattle may be high and the medical impact and first-instar larvae live in the eye annexes of animals and quite substantial. humans; Thelazia rhodesi is found in bovines. This nematode occurs on the surface of the cornea, under the nictitating The saliva of M. crassirostris has significant anticoagulant membrane, in the conjunctival sac and lacrimal duct. The activity (Lane & Crosskey, 1993); it is greater in females than worms are viviparous and first-stage larvae are passed by males, and greater in flies that have taken a bloodmeal than females into lacrimal secretions, where they are ingested by in newly emerged insects [Cornwall and Patton, 1914, quoted non-biting Diptera (Naem, 2007). First instars, free in the by Gooding (1972)]. Anticoagulant activity is likely to increase lacrimal secretion, are absorbed by secretophagous flies in the total loss of blood in animals on which this fly feeds (Van which they implement their development until they achieve the Emden, 1965). status of third-stage larvae and migrate to the labium from which they emerge and are released in the eye of a host In addition to its effects as an adult fly, M. crassirostris is (Otranto & Traversa, 2005). The lateral serration of the Thelazia responsible for some accidental intestinal myiases, in humans cuticle is responsible for mechanical damage to the conjunctival notably. Intestinal pseudoparasitism has been described after and corneal epithelium, which results in ocular discharge and the oral absorption of eggs and larval development in the increases worm transmission as flies feed on lacrimal secretions human digestive tract. This pseudoparasitism is rare and of containing first larval stages. Adult and larval stages of Thelazia little consequence. Patton attributed cases of intestinal myiases are thus responsible for eye disease, the symptoms of which observed in India to a ritual practice involving the consumption vary in severity and include lacrimation, ocular discharge, of five products of a cow, including fresh cattle dung [Patton, epiphora, conjunctivitis, keratitis, corneal opacity and ulcers. quoted by James (1947)]. Another circumstance occurs in cases Musca crassirostris is a known vector of T. rhodesia (Otranto of extreme poverty when people try to find undigested barley & Traversa, 2005). In India, Thelazia larvae were found in the grains in horse dung [Onorato, 1922, quoted by West (1951)]. thoraces of 1.6% of 4364 M. crassirostris, collected in January A similar case was reported from Italy (Hall & Smith, 1993). 1977 from cattle grazing in villages in the vicinity of Hyderabad; this was the first report of this fly species as an intermediate host Musca crassirostris as a vector of pathogens of Thelazia in southern India (Reddy & Rao, 1982). Similarly to non-biting flies, M. crassirostris is considered to be a mechanical carrier of pathogens, especially bacteria such © 2018 The Authors. Medical and Veterinary Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society, Medical and Veterinary Entomology, 33, 16–30

20 M. Desquesnes et al. A synergistic action of Thelazia, biologically transmitted, and Nearctic, Neotropical, Oriental and Palaearctic regions (Nihei & Mox. bovis (pinkeye), mechanically carried by M. crassirostris, de Carvalho, 2009). may occur. Indeed, Thelazia infection may create suitable con- ditions for Mox. bovis development; the symptoms of bacterial For species identification, a number of keys are available bovine keratitis caused by Mox. bovis are similar to those of the- (Patton & Patton, 1920; Patton, 1923; Patton & Senior-White, laziosis, and both diseases occur when secretophagous flies are 1924; Tumrasvin & Shinonaga, 1977; Couri et al., 2012). These present. The incidence of pinkeye increases proportionally to the are based on the following limited number of morphological density of the fly population (flies carry Mox. bovis) and pinkeye criteria: medium size, grey colour; the presence of four dark most probably develops on traumatic lesions caused by Thelazia longitudinal stripes (vitae) on the thorax (better marked in spp. (Otranto & Traversa, 2005). males); the grey–olive colour of the abdomen; eyes bare (widely separated in females); light orange palpi; a bare proepisternum Morphology and illustrated description and suprasquamal ridge; a large, shiny, boat-shaped proboscis; of M. crassirostris fully developed prestomal teeth, and a mid-tibia with a strong anteroventral seta on the middle third. Amongst its other aims, this review is intended to make the iden- tification of adult M. crassirostris easier in order to help field This section presents a fully illustrated description of the male technicians to recognize and consider its potential impact. and female adult M. crassirostris, including the main criteria used for their identification in the various keys available. The Morphology of larval stages of M. crassirostris species M. crassirostris is described below, based on reports in the literature (Patton & Cragg, 1913; Patton & Patton, The egg, larva and puparium are typical of Musca spp. 1920; Patton, 1923; Patton & Senior-White, 1924; James, 1947; (Crosskey, 1993). The eggs are large, measuring about Skidmore, 1985; Taylor et al., 2007) and completed by the 2.0–2.2 mm, of the form usual for M. domestica, cream in authors’ observations of over 100 flies trapped in Vavoua and colour, and smooth with a slightly concave dorsal surface Nzi traps (Laveissiere & Grebaut, 1990; Mihok, 2002) in various marked by a pair of parallel ribs (Muirhead Thomson, 1947). locations in Southeast Asian countries (Table 1). Thirty-three of The first-stage larva cannot be distinguished from that of these latter specimens were kept as vouchers at the Department M. inferior, and there is nothing distinctive about the form of of Entomology, Faculty of Agriculture, Kasetsart University the buccopharyngeal skeleton (Muirhead Thomson, 1947). The (Kamphaeng Saen, Nakhon Pathom Province, Thailand). These mature larva (third instar) is on average 10.5 mm in length; it included: two males and three females trapped on 5 December is of a deep lemon-yellow colour that, according to Patton & 2011 in Changmai, Thailand; three males and two females Cragg (1913), distinguishes it from the larvae of other species trapped on 22 November 2013 in Ipoh, Malaysia; five males and of Muscidae (although in the present authors’ observations, five females trapped on 17 December 2014 in Nakhon Pathom, Stomoxys larvae can also be yellow). The buccopharyngeal Thailand; four males and six females trapped on 7 October skeleton of the third instar is fairly similar to that of M. bezzii, 2015 in Nabong, Lao People’s Democratic Republic, and two but the left lateral hook is slightly smaller than the right hook, males and one female trapped on 18 January 2018 in Muñoz, and the anterior spiracles possess seven or eight finger-like Philippines. processes (James, 1947). The posterior spiracles are densely sclerotized, brownish, with a blackish peritreme, and present Body. Adult M. crassirostris are of medium size; males and as a kidney shape included in a D shape; they are separated by females are approximately the same size, about 5.5–7.5 mm in a distance of less than their width (Van Emden, 1965); each length, and may vary in colour from light to dark grey, with of them has three well-separated, paler, strongly sinuous slits typical olive–green tones (Fig. 1). This makes them relatively representing spiracular openings (Muirhead Thomson, 1947); easy to distinguish from other Musca (which are mostly black or the middle (outer) slits of the posterior spiracles are in approx- yellow in colour) when separating insects harvested using insect imately vertical positions (Van Emden, 1965) and exhibit four traps in the field. curves; the others are in approximately horizontal positions; the lower slit exhibits six curves, and the upper slit has four curves, Eyes. In living and fresh flies, the eyes are a brown–red the latter two of which flatten towards the median part. colour (burnt sienna, reddish brown) (Figs 1A and 2A, D), but the colour fades to dull brown when the insect is dead and Description of the adult stages of M. crassirostris dries (Figs 1B and 2B, E). The eyes are bare (thus differing from the hairy eyes of Musca lasiophthalma, and males of Adult flies trapped in the field should first be identified to the Musca convexifrons, Musca interrupta, M. bezzii and Musca genus; however, for the purposes of identifying species within formosana) (Tumrasvin & Shinonaga, 1977; Couri et al., 2012). the genus Musca, the reader is referred to a recent and complete The frons is very large in females (Fig. 2D) and very narrow in identification key. A total of 67 species in this genus have been males (Fig. 2A). The present authors observed that the frontal described, distributed in the Afrotropical, Andean, Australasian, index [calculated as the ratio of the smallest space between the eyes to the greatest length of the eye (Duvallet et al., 2017)] is 0.59–0.72 in females and 0.10–0.15 in males. Viewed from the side of the head, the border of the eye is straight (Fig. 2C), whereas in other Musca it is curved and convex (Fig. 2F). © 2018 The Authors. Medical and Veterinary Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society, Medical and Veterinary Entomology, 33, 16–30

The blood feeder Musca crassirostris 21 Table 1. Locations, dates and specimens of Musca crassirostris captured by the present authors in Southeast Asia, and vouchers conserved. Location Date Observed specimens Voucher specimens∗ Buriram, Thailand 14/01/2010 Males, females 2 males, 3 females Surin, Thailand 16/11/2010 Males, females Surat Thani, Thailand 15/06/2011 Males, females 3 males, 2 females Ratchaburi, Thailand 28/09/2011 Males, females Military camp, Chiang Mai, Thailand 05/12/2011 Males, females 5 males, 5 females Tha Wang Pha, Nan, Thailand 23/03/2013 Males, females 4 males, 6 females Nakhon Sawan, Thailand 01/05/2013 Males, females 2 males, 1 female Nakhon Si Thammarat, Thailand 26/06/2013 Males, females 3 males, 3 females Ipoh, Malaysia 22/11/2013 Males, females Yogyakrta, Indonesia 21/05/2014 Males, females Bogor, Indonesia 26/05/2014 Males, females Hanoi, Vietnam 28/11/2014 Males, females Nakhon Pathom, Thailand 17/12/2014 Males, females Nabong, Lao 07/10/2015 Males, females Kamphaeng Saen, Nakhon Pathom, Thailand 19/09/2016 Males, females Muñoz, Philippines 18/01/2018 Males, females Mindanao, Philippines 10/03/2018 Males, females ∗Vouchers kept at the Department of Entomology, Kasetsart University, Kamphaeng Saen Campus, Nakhon Pathom, Thailand. Fig. 1. Lateral views of (A) fresh and (B) dry specimens of Musca crassirostris. Antenna. The antenna is of a typical cyclorrhaphan type M. crassirostris: four large lateral teeth and four medium-sized and the arista has seven to 10 bristles on the dorsal side and five (two dorsal and two ventral) teeth can be seen (Fig. 4F). on the ventral side (Fig. 3). Maxillary palps are attached to the rostrum; they are charac- Mouthparts. In terms of their physiological position, teristically yellow–orange in colour (Fig. 4C, E, F) [most of the the mouthparts are folded up under the head; in a ventral Musca spp. other than M. conducens, M. planiceps, M. inferior view of the head, the labella are then usually visible, but and M. crassirostris have black palps (Patton & Senior-White, the teeth are not visible as they are hidden inside (Fig. 4A). In 1924)]. The maxillary palps are cylindrical in shape and nar- some cases, the labella are everted and the prestomal teeth are row towards their bases (Patton & Cragg, 1913; Walker, 1994) visible (Fig. 4B, C); however, in most specimens, it is necessary (Fig. 4F). to pull the mouthparts out to properly see the rostrum, palps and proboscis. When pulled out, the mouthparts show a very char- Thorax. The thorax varies in colour from smoke grey to a acteristic stout, bulbous proboscis with a boat-shaped, black, slightly yellowish grey, especially in females, and exhibits shiny mass of chitin: the mentum (also called the ‘haustellum’) four distinct dark longitudinal stripes (vitae), which are broad (Fig. 4C, D). This bears 6–8 long bristles, and 20–28 short and well marked in males (Fig. 5A), and narrow and more bristles (Fig. 4A–C). The labella harbours rasping prestomal lightly marked in females (Fig. 5B). The inner stripes are teeth greatly increased in size and strength compared with those interrupted before they reach the scutellum (around the mid- in other Musca spp. (Fig. 4C, E, F). This is characteristic of dle of the second thoracic segment). The propleuron is bare (Fig. 5C, white arrow), and the postalar ridge is without setulae. © 2018 The Authors. Medical and Veterinary Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society, Medical and Veterinary Entomology, 33, 16–30

22 M. Desquesnes et al. Fig. 2. Frontal view of the head in Musca crassirostris, in (A) fresh male, (B) dry male, (D) fresh female and (E) dry female specimens. Lateral views of the head in (C) M. crassirostris and (F) Musca domestica. The anterior spiracle is light brown to beige (Fig. 5C, grey arrow). It has been described as ‘dark brown’ in specimens from Namibia (Couri et al., 2012); however, in the present specimens from Thailand, Malaysia, Indonesia, Philippines, Vietnam and Lao, no such colour was observed and only light brown colouring was seen. Similarly, in five specimens caught in 1993 in the northern semi-desert area of Ngurunit, Kenya (Mihok et al., 1995), the anterior spiracle was of a light brown colour (Steve Mihok, personal communication, 2017). The suprasquamal ridge is bare (Fig. 5D, black arrow); two anterior sternopleural bristles are present. The thoracic chaetotaxy (macrochaetae) was completely described by Patton & Cragg (1913); there are three sternopleural bristles, arranged in a ‘1 : 2’ pattern (see sternopleural bristle 1 : 2 in Fig. 6A). Fig. 3. Musca crassirostris: lateral view of the antenna and arista. Wings. The wings are pale grey and yellowish at the anterior edges; they harbour some black bristles at the base of the costa © 2018 The Authors. Medical and Veterinary Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society, Medical and Veterinary Entomology, 33, 16–30

The blood feeder Musca crassirostris 23 Fig. 4. Musca crassirostris. Ventral views of the head with (A) labella visible, teeth not visible and (B) labella everted, teeth visible. (C) Side view of the proboscis showing detail of the mentum and prestomal teeth (labella everted). Lateral views of the head, with (D) the proboscis pulled out and (E) the prestomal teeth visible. (F) Detail of the prestomal teeth. Fig. 5. Musca crassirostris. Dorsal views of the thorax (wings removed) in (A) male and (B) female specimens. (C) Lateral view of the thorax and head (white arrow: propleuron; grey arrow: spiracle). (D) Detailed view of calypters (the black arrow points to the bare suprasquamal ridge). © 2018 The Authors. Medical and Veterinary Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society, Medical and Veterinary Entomology, 33, 16–30

24 M. Desquesnes et al. Fig. 6. Musca crassirostris. (A) Lateral view of the thorax (the black arrows point to one anterior and two posterior sternopleural bristles). (B) Basal part of the wing, showing black bristles at the base and black hair along the costa. (C) Annotated image of the wing. and several rows of black hair along them (Fig. 6B). Their vena- brown–black longitudinal stripe pointing backwards but not tion is similar to that in most other Musca, but the M vein (fourth reaching the lower edge; segment 3 has a dark longitudinal longitudinal vein, or m1 + 2) bends up at a sharper angle (almost median band, extending almost the whole length of the segment, a right angle) to reach the costa anteriorly to the apex, very and segment 4 has a faint dark, longitudinal median band, close to the third longitudinal vein (R4 + 5), at a distance below extending the whole length of the segment (Fig. 7C) (Patton & the length of the r–m cross vein; vein r1 is bare, and the anal Cragg, 1913). vein does not reach the wing margin (James, 1947). The discal cell is delimited anteriorly by a proximal dm–cu vein (Fig. 6C). In females, the abdomen is olive or greyish-yellow to green, and is longer than it is wide with a width : length ratio of Abdomen. The abdomen shows four segments which may or around 0.7; it has black bristles that are regularly spread all not alternate in black and light markings (Taylor et al., 2007). over the mesopleuron and sternopleuron, but are absent from Indeed, the abdomen may appear to be mostly greyish when the the hypopleuron (different from calliphorid flies). The middle insect is unfed (Figs 7 and 8A), but when it is distended by the line of segment 1 has no mark or a small darker area anteriorly; bloodmeal, very dark and shiny anterior parts of the sternites and segment 2 has a narrow longitudinal band; segment 3 has an tergites (2–4) appear between the abdominal segments, giving incomplete band, and segment 4 has no band (Fig. 7A) (Patton the abdomen a transversally striped appearance (Fig. 8B). In & Cragg, 1913). The ovipositor is slender with two dark cerci both sexes, on the dorsal abdomen, darker areas can be seen on at the extremity (Fig. 8C). The cerci are well developed, and are the lateral sides of segments 2 and 3, whereas segment 4 appears either sub-cylindrical with an inner surface that is sclerotized mostly darker; the median area is different in males and females. and haired on the apical half, or compressed with an inner surface that is membranous and without hairs (Huckett & In males, the abdomen is grey, of a heart shape, with a Vockeroth, 1987). width : length ratio close to 1 (Fig. 7C, D). Segment 1 has a dark, almost black, transverse patch extending to the sides Legs. The legs are mostly of a dark greyish colour, with strong but not reaching the hind margins; segment 2 has a triangular bristles on the ventral and dorsal parts of the fore femur (L1) © 2018 The Authors. Medical and Veterinary Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society, Medical and Veterinary Entomology, 33, 16–30

The blood feeder Musca crassirostris 25 Fig. 7. Musca crassirostris. Dorsal views of the abdomen in (A) female and (C) male specimens. Ventral views of (B) female and (D) male specimens. (Fig. 1A) and the dorsal part of the hind femur only (L3); the Tyagi & Baqri, 2005; Huang et al., 2007; Dorrah, 2009; Chin fore tibia are without ventral setae in the apical half; the mid et al., 2010; ElMahi, 2011; Al-Saffar et al., 2012; Couri et al., tibia (L2) has a characteristic strong bristle (like a spur) pointing 2012; Moradi et al., 2013). medially and located about two-thirds of the distance towards the distal end of the tibia (Fig. 8D, black arrow), as well as two Musca crassirostris was recently captured in traps by the medial and one external spur at its distal extremity (Fig. 8D). present authors in Thailand, Malaysia, Lao, Vietnam, Indonesia and the Philippines (Table 1). Reports and surveys of M. crassirostris Surveys of M. crassirostris in Thailand Reports Trapping studies using Nzi and Vavoua traps were con- ducted recently in Thailand, Malaysia, Indonesia, Lao, Musca crassirostris is widely distributed from Africa through Vietnam and Philippines under the auspices of an informal the Middle East, to Southeast Asia (James, 1947). A more consortium of researchers in Southeast Asia [the GREASE detailed geographical distribution is difficult to establish (Gestion des Risques Epidémiologiques Emergents en Asie because there are numerous but most often anecdotal reports du Sud Est) network and the BioZoonoSEA platform]. of M. crassirostris. A non-exhaustive list of reports found in These have reported very high numbers of M. crassirostris the literature is presented in Table 2, with reference to the in various workshops [http://www.grease-network.org/ authors (Patton & Patton, 1920; Patton, 1922, 1923; Du Toit content/download/4694/35193/version/1/file/REPORT_BIVT_ & Nieschlutz, 1933; James, 1947; Muirhead Thomson, 1947; Workshop_Malaysia2013.pdf, http://umr-intertryp.cirad.fr/ Mellor, 1978; Sucharit & Tumrasvin, 1981; Kigaye & Giffar, content/download/4379/32694/version/1/file/25+-+29th+ 1991; Shinonaga & Singh, 1994; Dia, 1997; Veer et al., 2002; © 2018 The Authors. Medical and Veterinary Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society, Medical and Veterinary Entomology, 33, 16–30

26 M. Desquesnes et al. Fig. 8. Musca crassirostris. Side views of the abdomen in (A) unfed and (B) blood-fed specimens. (C) Female ovipository (externalized). (D) Mid-leg, showing a bristle two-thirds along the distal tibia (black arrow). novembre+2014+Vietnam.pdf, http://umr-intertryp.cirad times more abundant than Stomoxys spp. and tabanids, respec- tively; this study also suggested that Malaise traps are highly .fr/content/download/4410/32978/version/1/file/FINAL+ effective in catching Haematobia and M. crassirostris. PROGRAM+Workshop+LAO.pdf, https://www.grease- The authors of the present paper also carried out an original study at the Kamphaeng Saen Campus of Kasetsart University, network.org/content/download/5562/41475/version/1/file/ Nakhon Pathom Province, using one unbaited Vavoua trap and one Nzi trap set up 1 day per week, during April–June 2016, FINAL+REPORT+OW%26TW+at+PCC050218.pdf, https:// in the vicinity of a beef cattle stable with six feeder cattle. Traps were set up at 20 m from the stable, 100 m apart and www.grease-network.org/meetings-workshops2/workshops- were set at 06.00 hours and removed at 19.00 hours (cages were changed every 2 h) to record the daily activity pattern of the meetings/2018/diagnosis-and-control-of-trypanosomes-and- flies (to be reported elsewhere). Over 3 months, 12 946 flies were trapped; on average, the relative abundances of the flies, their-vectors-in-animals-and-humans-in-sea (all accessed on by increasing numbers, were: tabanids 0.7%; Stomoxys spp. 7.8%; M. crassirostris 33.0%, and M. domestica 58.4%. Hence, 3 May 2017)]. In around a fifth of cases, the dissection of M. crassirostris was four and 45 times more abundant than Stomoxys spp. and tabanids, respectively. Detailed results of freshly captured M. crassirostris showed the presence of fresh these studies are presented in Table 3. During this study, direct observations of fly annoyance were made on the six feeder cattle blood in the guts, confirming the haematophagous character kept inside the stable. During tail flick records (made to evaluate global insect annoyance; to be reported elsewhere), for 3 min of the species. In a study carried out in Nigeria, 100% of on each cow in the morning and evening, Stomoxys spp. and M. crassirostris were observed mostly on the legs of the cattle. specimens caught on lions and hyenas were blood-fed (Dipeolu, Musca crassirostris appeared to be at least three times more abundant than Stomoxys spp., and the defensive movements 1976); however, the trapping method (insects were caught in of the animals were clearly linked to the flies’ landing and blood feeding. Meanwhile, M. crassirostris was also regularly the cages of the animals) differs from the trapping techniques used in the present studies (field surveys). The high abun- dance, haematophagous character, and high bovine affinity of M. crassirostris strongly suggest that its impacts on livestock should be reconsidered. It should not be considered merely as ‘another sponging fly’, with little presumed impact. In a recent study, carried out in five dairy farms in Saraburi Province, Thailand, using non-baited Malaise traps for 1 day per month, from June 2008 to October 2009, 100 403 flies were trapped; the relative abundances of flies, by increasing num- bers, were: tabanids 0.2%; Haematobia spp. 0.4%; M. domestica 2.0%; Stomoxys spp. 24.4%, and M. crassirostris 73.0% (Phasuk et al., 2010, 2013). Hence, M. crassirostris was three and 348 © 2018 The Authors. Medical and Veterinary Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society, Medical and Veterinary Entomology, 33, 16–30

The blood feeder Musca crassirostris 27 Table 2. Reports of occurrences of Musca crassirostris: regions, countries, areas and references. Region Country or area References East Asia Southeast Asia China Sucharit & Tumrasvin (1981) Shantung (China) James (1947) South Asia Taiwan Huang et al. (2007) Japan Huang et al. (2007) Middle East All James (1947) Burma Sucharit & Tumrasvin (1981) North Africa Thailand Sucharit & Tumrasvin (1981); present paper West Africa Lao present paper East Africa Vietnam James (1947); present paper Central Africa Malaysia Chin et al. (2010); present paper South of Africa Indonesia, Borneo, Java, Sumatra, Lombok Huang et al. (2007) Europe Java (Indonesia) Present paper Philippines Patton (1923); James (1947); present paper India Patton (1922) Assam (India) Thomson (1947) Orissa (India) Veer et al. (2002) Thar Desert (India) Tyagi & Baqri (2005) Nepal Shinonaga & Singh (1994) Sri Lanka Huang et al. (2007); Sucharit & Tumrasvin (1981) Pakistan Patton (1922) Iran Moradi et al. (2013) All James (1947) Caucasian Russian republics Sucharit & Tumrasvin (1981) Georgia, Armenia, Azerbaidjan Sucharit & Tumrasvin (1981) Turkey Patton & Patton (1920) Cyprus James (1947) Lebanon, Palestine, Israel Patton (1922) Syria Patton (1922) Iraq Al-Saffar et al. (2012) Jordan, Mesopotamia Patton & Patton (1920) Arabian peninsula James (1947) Oman, including Dhorfar Mellor (1978); ElMahi (2011) Socotra island (Yemen) Al-Saffar et al. (2012) All Dia (1997) Egypt Dorrah (2009) Sinai peninsula (Egypt) James (1947) Libya Dorrah (2009) Mauritania, Cape Verde Dia (1997) Senegal Dia (1997) Ghana Dorrah (2009) Ethiopia, Sudan Kigaye & Giffar (1991) Congo Kigaye & Giffar (1991) Zambia, Zimbabwe, Namibia Couri et al. (2012) South Africa Du Toit & Nieschlutz (1933) Dodecanese Islands (Greece) Patton & Patton (1920); James (1947) reported to attempt to feed on the technicians making the emphasize the need for further evaluation of this species’ poten- observations, although not on intact skin and only on previously tial annoyance and direct impact on livestock. wounded skin areas at which blood was visible (either due to scratches or previous Stomoxys bites); M. crassirostris was Conclusions obviously attracted by the blood in these observations. This review and description of M. crassirostris highlights a In a study carried out in India, M. crassirostris represented rather neglected but very much present fly, especially on 17% of the haematophagous insects trapped (Veer et al., 2002); bovine farms. Seasonally in phase with the true biting flies, in another study conducted in South Africa, the relative abun- M. crassirostris is an obligate and true haematophagous fly, even dance of M. crassirostris was 20% vs. 11 other Musca spp. if it may rely on the activities of true biting flies to successfully (Nevill, 1997). Although made in various locations, seasons and obtain most of its bloodmeals. Although very little attention using various trapping methods, all these observations show very has so far been paid to this fly, it is highly recommended that high relative abundances of M. crassirostris in comparison with M. crassirostris be identified and distinguished from the true other haematophagous flies, especially in bovine farms, and thus © 2018 The Authors. Medical and Veterinary Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society, Medical and Veterinary Entomology, 33, 16–30

28 M. Desquesnes et al. Table 3. Detailed results of trapping surveys carried out in two References provinces in Thailand. Al-Saffar, H., Augul, R., Ali, H. & Rassoul, M. (2012) Occurrence of Saraburi, Kamphaeng Saen, adult muscid flies on sticky traps in some Iraqi provinces. Bulletin of the Iraq Natural History Museum, 12, 1–9. Saraburi Nakhon Pathom Baldacchino, F., Muenworn, V., Desquesnes, M., Desoli, F., Charoen- Province, Province, 2016, viriyaphap, T. & Duvallet, G. (2013) Transmission of pathogens by Stomoxys flies (Diptera, Muscidae): a review. Parasite, 20, 26. 2008–2009, Vavoua and Baldacchino, F., Desquesnes, M., Mihok, S., Foil, L.D., Duvallet, G. & Malaise traps∗ Nzi traps† Jittapalapong, S. (2014) Tabanids: neglected subjects of research, but important vectors of disease agents! Infection Genetic and Evolution, Total pest insects trapped, n 100 403 12 946 28, 596–615. Tabanids, n 215 96 Stomoxys spp., n 24 969 1012 Bernier, U.R., Hoel, D.F., Hogsette, J.A., Hanafi, H.A. & Kline, D.L. Haematobia ssp., n 410 2 (2008) Effects of lures an trap placement on sand fly and mosquito Musca crassirostris, n 74 809 4277 traps. Sixth International Conference on Urban Pests, Budapest, Musca spp. other than 2051 7561 13–16 July 2008, pp. 171–175. M. crassirostris, n 348 45 Bitome Essono, P.Y., Dechaume-Moncharmont, F.X., Mavoungou, J., Ratio of M. crassirostris : tabanids 3 4 Obiang Mba, R., Duvallet, G. & Bretagnolle, F. (2015) Distribution Ratio of and abundance of hematophagous flies (Glossinidae, Stomoxys, and Tabanidae) in two national parks of Gabon. Parasite, 22, 23. M. crassirostris : Stomoxys spp. Borror, D. & White, R. (1970) . A Field Guide to the Insects of America ∗Phasuk et al., 2010, 2013. North of Mexico. Houghton Mifflin, Boston, MA. †This study. de Carvalho, C.J.B., Couri, M.S., Pont, A., Pamplona, D.M. & Lopes, sponging flies that are considered to be of lower impact as S.M. (2005) A catalogue of the Muscidae (Diptera) of the Neotropical a result of their facultative blood feeding and lack of rasp- region. Zootaxa, 860, 1–282. ing mouthparts. The fly can be rapidly identified based on the shape and colour of its abdomen and the peculiar shape of Chin, H., Ahmad, N., Kian, C. et al. (2010) A study of cow dung its brilliant, stout proboscis; this readily distinguishes it from Diptera in Sentul Timur, Kuala Lumpur, Malaysia. Journal of Tropical non-rasping, sponging flies. The identification and counts of this Medicine and Parasitology, 33, 53–61. fly in regular trapping of livestock pests are strongly recom- mended to evaluate its potential impact. Through these activities, Couri, M.S., de Carvalho, C.J.-B. & Pont, A. (2012) Taxonomy of the it may become apparent that M. crassirostris should be con- Muscidae (Diptera) of Namibia: a key to genera, diagnoses, new trolled together with tabanids and Stomoxys spp. Adapted tools records and description of a new species. African Invertebrates, 53, currently under development for the control of Stomoxys spp. 47–67. and tabanids [the Flyscreen project/French National Research Agency (ANR)] should then be jointly considered for the control Crosskey, R.W. (1993) Stable-flies and horn-flies (bloodsucking Mus- of biting flies and M. crassirostris. cidae). Medical Insects and Arachnids (ed. by R.P. Lane & R.W. Crosskey), pp. 289–401. Springer, Dordrecht. Acknowledgements Desquesnes, M. (2004) . Livestock Trypanosomoses and their Vectors in The authors wish to thank Jumnongjit Phasuk, Department Latin America. CIRAD-EMVT Publication, Office International des of parasitology, Faculty of Veterinary Medicine, Kasetsart Épizooties (OIE), Paris. University, Bangkok, Thailand, for sharing information on Musca crassirostris and other haematophagous insect trap- Dia, M. (1997) Epidemiologie de la trypanosomose cameline à Try- ping studies in the Saraburi area, Alan Dargantes, Central panosoma evansi en Mauritanie. PhD Thesis, Montpellier University, Mindanao University, University Town, Musuan, Philippines, Montpellier. for sharing M. crassirostris specimens from Mindanao, and Steve Mihok for advice, the revision of their English-language Dipeolu, O.O. (1976) The biting flies in the zoo of the University of manuscript, and for complementary information and the shar- Ibadan. East African Wildlife Journal, 14, 229–232. ing of M. crassirostris specimens. The authors would also like to thank the Department of Entomology, Faculty of Agri- Dorrah, M.A. (2009) Purification and characterisation of Chymotrypsin culture at Kamphaeng Saen and the Faculty of Veterinary isolated from the midgut of two cyclorraphan larvae. Efflatounia, 9, Medicine, Kasetsart University, Thailand, for support and lab- 1–9. oratory expenses and access, and for keeping the voucher spec- imens of these flies. This work was funded by the Centre de Du Toit, R. & Nieschlutz, O. (1933) Musca crassirostris, a bloodsucking Coopération Internationale en Recherche Agronomique pour le fly new to South Africa. Journal of the South African Veterinary Développement (CIRAD) and the French National Research Association, 4, 97–98. Agency [Agence Nationale de la Recherche (ANR)], under the ‘FlyScreen’ project (ANR-15-CE35-0003). The authors declare Duvallet, G., Baldacchino, F. & Desquesnes, M. (2017) Stomoxyini no conflicts of interest. (Diptera: Muscidae: Muscinae). Entomologie Médicale et Vétérinaire (ed. by F.R. Duvallet)), pp. 391–403. IRD Editions, Marseille, Versailles. ElMahi, A.T. (2011) Hematophagous flies in Dhofar (Sultanate of Oman): a limiting factor and a potential pathogenic vector. Agricul- tural and Marine Sciences, 16, 65–73. Gill, B. (1977) . Trypanosomes and Trypanosomiases of Indian Live- stock. Indian Council of Agricultural Research, New Delhi. Gooding, R.H. (1972) Digestive process of haematophagus insects. I. A literature review. Quaestiones Entomologicae, 8, 5–60. © 2018 The Authors. Medical and Veterinary Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society, Medical and Veterinary Entomology, 33, 16–30

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